Chen-Zhu Wang

Root volatiles mediate diverse belowground interactions among plants, microbes, and invertebrates, but biological and environmental conditions strongly influence their production, movement, perception, and ecological effects. This review synthesizes current knowledge through an integrative conceptual framework linking five dimensions: (1) chemical diversity and biosynthesis; (2) regulation by biotic and abiotic factors; (3) plant internal signaling and resource allocation; (4) ecological adaptation and reciprocal evolutionary interactions with soil organisms; and (5) implications for agricultural management. Key roles include defense against herbivores and pathogens, recruitment of beneficial microbes and natural enemies, plant recognition, allelopathy, systemic signaling between roots and shoots, and coordination across multitrophic networks. The synthesis examines how volatile identity and concentration, soil properties, microbial transformation, and plant genotype influence signal transmission and ecological outcomes. Comparisons across taxa, compounds, and experimental systems clarify which mechanisms are broadly supported and which remain context‐dependent. Priorities include resolving molecular pathways, tracing volatile transport and persistence in soil, distinguishing volatile effects from those of nonvolatile exudates, and validating functions under field conditions. A deeper mechanistic and ecological understanding of root volatiles is therefore essential for developing resilient crop protection strategies, reducing dependence on agrochemical inputs, advancing sustainable agroecology, and sustaining long‐term soil health.

Helicoverpa armigera is a typical polyphagous species whose larvae primarily bore in flower buds and fruits of host plants, causing serious damage to many crops. Olfaction plays a key role in host selection, but the molecular basis of olfactory perception in larvae is poorly understood. Herein, we identified a highly expressed odorant receptor, HarmOr54, in larval antennae through qRT-PCR and in situ hybridization experiments. Drosophila T1 neurons expressing HarmOr54 ectopically showed specific responses to (-)-bornyl acetate and 2-ethylhexyl acetate. CRISPR/Cas9-generated homozygous mutant larvae lost avoidance to (-)-bornyl acetate, unlike wild-type larvae, while 2-ethylhexyl acetate showed no behavioral effect. Structural modeling and docking revealed that both ligands bound to the same HarmOr54 pocket, but (-)-bornyl acetate displayed stronger binding affinity. These findings enhance our understanding of the olfactory mechanisms in lepidopteran larvae and provide new insights into pest control strategies targeting the larval stage.

Parasitoids are vital biological control agents in agricultural pest management, with mating and parasitism as their core behaviors essential for reproduction and survival. In recent decades, advanced analytical techniques, such as gas chromatography-electroantennographic detection (GC-EAD), have enabled the identification of key semiochemicals that regulate parasitoid behavior. Notably, studies on Campoletis chlorideae (Hymenoptera: Ichneumonidae) have elucidated the mechanisms of sex pheromone communication, advancing our understanding of pheromonal signaling in parasitoids. Moreover, plant-derived synomones and host-derived kairomones serve as pivotal chemical cues for host location, underpinning tritrophic (plant–pest–parasitoid) interactions. The functional characterization of olfactory receptors tuned to herbivore-induced plant volatiles and kairomones, achieved through ectopic expression systems, has further clarified the molecular mechanism underlying semiochemical-mediated behaviors. Synthetic biology offers promising avenues for manipulating parasitoid behavior by leveraging genetic and metabolic engineering of plants and yeast to release critical synomones and kairomones, thereby improving parasitoid recruitment. This review synthesizes the role of semiochemicals in mediating parasitoid behaviors, evaluates methodologies for behavioral manipulation, and explores the potential and limitations of integrating synthetic biology with semiochemicals to advance sustainable pest management.

The majority of pheromone receptors (PRs) in the cotton bollworm Helicoverpa armigera have been deorphanized, but the function of HarmOR11, a PR highly expressed in both male and female antennae, has remained controversial. We expressed HarmOR11 in Drosophila T1 neurons and found that the neurons respond to plant volatiles benzyl acetate, methyl phenylacetate, and methyl benzoate. When we knocked out HarmOR11 by CRISPR-Cas9, the type A sensilla on the male antennae lost responsiveness to all the three compounds and the enhancing effect of the three compounds on behavioral responses of males toward the sex pheromone disappeared; the trichoid sensilla on female antennae responsive to all the three compounds, originally accounting for 15.38% on wild-type antennae, were no longer responsive, and female preference for oviposition in proximity to these compounds significantly decreased. The discovery advances understanding of PR function evolution and provides new opportunities for enhancing the attractiveness of pheromone traps.

BACKGROUND: Chemosensory detection of sugars is crucial to the feeding and oviposition of herbivorous insects. The fall armyworm Spodoptera frugiperda is an invasive polyphagous insect in China, but its molecular and regulatory basis of sugar perception remains elusive. In this study, we investigated the molecular mechanism for sugar sensation in this species.RESULTS: The phylogenetic analysis found that sugar gustatory receptors (GRs) formed species‐specific branches, and Group II sugar GRs are highly conserved, with the highest identity between SfruGR6 and HarmGR6. The oocyte expressing SfruGR6 responded to fucose and sucrose by using the Xenopus oocyte expression system. The larval sensilla styloconica have fucose‐sensitive gustatory receptor neurons (GRNs), and the neural firing rates from medial sensilla styloconica towards fucose were higher than that in lateral sensilla styloconica. Fucose acts as a feeding stimulant, while sustained feeding of fucose caused the reduction of larval weight and the survival rate of female adults, but had no effect on the pupa weight and period. Ingestion of fucose alters the composition and abundance of gut microbiota in larvae, resulting in the abundance increase of Exceevirus Xc38, Escherichia coli, Klebsiella pneumoniae, and the decrease of Enterococcus casseliflavus, Microbacterium sp. Be9, Enterococcus faecium, and Enterococcus mundtii.CONCLUSION: These findings reveal that SfruGR6 is a sugar GR tuned to fucose and sucrose, and ingestion of fucose negatively affects growth and survival by regulating gut microbiota in S. frugiperda. This work not only enriches the knowledge of co‐evolution between insects and plants, but also provides new insights into pest control strategies. © 2025 Society of Chemical Industry.

Pieris butterflies recognize host Brassicaceae plants via sensing glucosinolates, but the molecular mechanism remains unclear. Here, we cloned five gustatory receptor genes highly expressed in larval mouthparts, adult foreleg tarsi, and the proboscis of Pieris rapae and then ectopically expressed each of them in Gr5a neurons of Drosophila and determined responses of the neurons to glucosinolates. Among them, only Gr5a > PrapGr19 neurons respond to gluconapin dose-dependently. Knockdown of PrapGr19 by 52.3% significantly reduces the firing rate of the lateral sensilla styloconica in the fifth instar larvae of P. rapae to gluconapin but has no effect on the responses to sinigrin and sucrose. This leads to the loss of the feeding preference of larvae for gluconapin and Cleome spinosa. All these results indicate PrapGr19 is the receptor mediating P. rapae larvae sensing gluconapin, which provides new knowledge for revealing molecular bases of glucosinolate sensing in Pieris butterflies.

BACKGROUND: Contact chemoreception plays a crucial role in host–plant recognition and acceptance of herbivorous insects; however, the mechanisms by which peripheral taste inputs regulate insect feeding remain unclear. The aim of this study is to clarify the ecological significance of sugar and bitter gustatory receptors (Grs) in the relationship between Helicoverpa armigera and its hostplants.RESULTS: Blocking the positive input via knocking out Gr10 only leads to an increase in palpating frequency, and decreases in both the feeding time and the amounts of larvae on palatable fruit substrates, thereby prolonging the larval stage. Blocking the positive input via knocking out Gr6 only results in a decreased percentage of the proboscis extension reflex (PER) to sucrose and a reduced sucrose intake of adults, thus weakening their ability to detect nectar and decreasing longevity and fecundity. Blocking the negative inputs via knocking out Gr180 decreases palpating frequency and increases both feeding time and amount on unpalatable leaf substrates, leading to early larval mortality and a loss of aversion in adults to coumarin.CONCLUSION: These results indicate that Gr10 is crucial for larvae and Gr6 for adults in tasting some palatable foods, while Gr180 is important for both larvae and adults in avoiding some unpalatable foods. These findings enhance the understanding of how feeding behavior is controlled by taste neuron input in this polyphagous moth species. © 2025 Society of Chemical Industry.

Myo-inositol, a sugar alcohol produced by most plants, serves as a nutrient and feeding stimulant for many phytophagous insects. Inositol-sensitive taste sensilla have been characterized in many Lepidoptera larvae, but their molecular bases remain unclear. In this study, we determined the gustatory receptors (GRs) for myo-inositol in larva of Helicoverpa armigera, a worldwide crop pest. First, electrophysiological analyses revealed that medial sensilla styloconica strongly responded to myo-inositol and ribose, with weaker responses to xylose, and one GRN inside sensillum may mediate the response to these three chemicals. Based on phylogenetic analysis of sugar GRs of Lepidoptera insects and previous results on Bombyx mori, we then selected two candidate GRs, HarmGR13 and HarmGR11. Using CRISPR-Cas9, we generated knockout mutants for the two GR genes. Knocking out HarmGR13 abolished the responses of the sensilla to myo-inositol, ribose, and xylose, while knocking out HarmGR11 showed no changes. Behavioral assays confirmed that larvae of HarmGR13 homozygous mutant lost the feeding preference to myo-inositol which the wild-type larvae had. Further functional analysis with Xenopus oocytes expressing system and two-electrode voltage-clamping demonstrated that myo-inositol and ribose specifically induced concentration-dependent currents in HarmGR13-expressing oocytes. Structural predictions and molecular docking of HarmGR13 revealed three amino acid residues might be involved in ligand binding. Mutation of these residues resulted in loss of oocyte responses to myo-inositol and ribose. We reveal that HarmGR13 is a receptor that mediates the activity of the cells sensitive to inositol and ribose in larvae, providing new molecular targets for the strategy of regulating the feeding behavior of pests by modifying taste.

Interspecific interactions are crucial for maintaining ecological balance. Foraging and food consumption are fundamental for the survival of animals. In natural environments, wild rodents feed on various insect species, including moth larvae, and odor-guided evaluation of potential food resources is a critical step in initiating feeding behavior. However, the mechanisms by which rodents seek and feed on insect prey remain poorly understood. Herein, we employed a laboratory-based predator-prey interaction system using mice and cotton bollworm larvae to investigate the neural mechanisms underlying food-seeking and feeding behaviors at both cellular and neural circuit levels. We demonstrate that mice exhibit a strong preference for consuming fed larvae, and this preference is dependent on the main olfactory system. Gas chromatography-mass spectrometry (GC-MS) analysis revealed significant differences in the chemical profiles of fed and unfed larvae, with fed larvae containing a higher level of linoleic acid (LA) and a lower level of (Z)-9-tricosene ((Z)-9-TE). Behavioral assays showed that mice, as well as Brand’s voles and brown rats, are attracted to LA but avoid (Z)-9-TE in a two-choice odor preference test. Furthermore, we identified that the dopaminergic pathway from the ventral tegmental area (VTA) to the medial olfactory tubercle (mOT) plays a central role in mediating this preference. Chemogenetic inhibition of this pathway abolished the preference for LA over (Z)-9-TE, while chemogenetic activation reversed this effect. Additionally, fiber photometry recordings and pharmacology revealed that mOT D1 and D2 spiny projection neurons (SPNs) preferentially mediate attraction to LA and avoidance of (Z)-9-TE, respectively. These findings provide a framework for rodents’ food forage and consumption in the complicated natural environment.

Sex pheromone communication is an essential component of mate recognition in moths. In this study, we heterologously expressed male-biased pheromone receptors (PRs) of diamondback moths, Plutella xylostella, in Drosophila OR67d neurons and determined their responses toward sex pheromonal compounds. The neurons expressing PxylOR59, PxylOR13, and PxylOR46 specifically responded to three sex pheromone components, Z11-16:Ald, Z11-16:Ac, and Z11-16:OH, respectively. The most effective ligands of other three PRs, PxylOR47, PxylOR49, and PxylOR73 were Z11-14:Ac, Z9,E12-14:Ac, and Z9,E11-14:Ac, respectively. Interestingly, the last two PRs were also tuned to Z11-14:Ac, which was not present in the pheromone glandular extract of P. xylostella in previous studies. Y-tube olfactometer assays revealed that the sex pheromone blend mixed with Z11-14:Ac at a ratio of 100:0.1 attracted more virgin males compared to the sex pheromone blend. These findings improve our understanding of the olfactory coding mechanisms in this important pest and provide promising potential for enhancing insect capture of pheromone traps.